Sugar competition is important for sheath blight resistance in rice towards climate adaptation

Sheath blight (ShB) caused by Rhizoctonia solani Kühn is one of the most serious diseases in rice and is highly susceptible to climate and environmental influences, high humidity climate conditions combined with higher temperatures often lead to more severe occurrences of ShB. The heterotrophic R. solani and rice might compete for sugar at the border of interaction; however, the underlying mechanism remains unclear. In this study, we demonstrated that the expression level of Sugar will eventually be exported transporters (SWEETs) induction was higher in ShB susceptible varieties than in ShB resistant varieties by R. solani inoculation. Inoculation of R. solani revealed that most sweet mutants were less susceptible to ShB than the wild-type. Also, sugar transporters (STPs) gene expression was sensitive to R. solani infection. STPs were localized at the plasma membrane and transported hexose in yeast. Knockdown of STP4 increased the susceptibility of rice to ShB. Interestingly, sequence analysis identified two monosaccharide transporter genes (hereafter named RsMST). RsMSTs transported 2-deoxyglucose, a toxic glucose analog in yeast, suggesting their role as glucose transporter. Spray-induced gene silencing of RsMST1 or RsMST2 dramatically suppressed their expression level and reduced virulence of R. solani. These data suggested that R. solani might induce SWEETs to efflux sugar from the cytosol to apoplast, and STP and RsMSTs compete for sugar at the apoplast for host defense and pathogen virulence. This study provided important insights for ShB-resistant breeding in rice.